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A boy and his dog (names chosen by the player) leave a movie theater in the small town of Podunk when the dog chases a cat into an abandoned mansion. In the mansion the boy finds a strange machine that teleports him to an unknown location, seemingly a space station. The boy is herded onto an escape craft that crashes on the planet, where he finds a large jungle full of dinosaurs and man-eating plants.

The boy explores the jungle and finds a group of humans led by a young girl named Elizabeth. Elizabeth agrees to help the boy if he rescues the village alchemist, Strong Heart, from a swamp called Bugmuck. The boy does so, and Elizabeth reveals she is from Podunk as well. The mansion the boy entered belonged to her grandfather, Professor Ruffleberg, and he had built a machine that could transport people to worlds of their imagination. This region, Prehistoria, is based on her fascination with cave people and dinosaurs. Elizabeth can still sense outside influences, though, and believes someone is active in the nearby volcano.

In the volcano the boy finds an evil copy of Elizabeth has taken control of the dinosaurs in the area and is planning to shut down the volcano, causing an ice age. The boy defeats her monster, Magmar, and the girl overloads the volcano to make it erupt. The eruption lands the boy in a new region, Antiqua, based on ancient Greek, Roman, and Egyptian civilization, and when he awakens his dog has gone missing. The boy crosses the desert to Nobilia, where his dog has become revered as a sacred animal and "chooses" him to fight in the coliseum. When the boy is victorious, the ruler of Nobilia's aide orders him to retrieve two ancient jewels, the Diamond Eyes, from the ruins across the river, and their ruler will send the boy home if he does.

The Boy explores the desert outside Nobila.

Across the river the boy meets an archaeologist, Horace Highwater, who was a friend of Ruffleberg. This area, Antiqua, is a product of his imagination. Horace says that the ruler of Nobilia cannot be trusted, and has only recently taken over the city but has never been seen in public. Horace aids the boy in exploring the nearby Hall of Collosia and Pyramid to retrieve the Diamond Eyes, and on returning to Horace's camp finds he is gone. On the way to Nobilia Horace intercepts the boy and takes the Diamond Eyes, but the boy notices he was acting odd. In Nobilia, "Horace" uses the Diamond Eyes to revive the town statue as a giant monster, Aegis.

When Aegis is destroyed, the real Horace arrives and explains that the ruler of Nobilia was an evil, robotic copy of him. Aegis' power core is about to explore, so the town strongman, Tiny, hurls it away. The explosion opens up an underground tunnel that leads to a new area, Ivor Tower, a medieval kingdom. In Ivor Tower the boy wins an audience with the ruler, Queen Bluegarden. The Queen is another member of Ruffleberg's experiment, and asks for the boy's help in clearing out the neighboring kingdom of Ebon Keep of a few stragglers that refuse to move to Ivor Tower.

In Ebon Keep the boy finds a woman identical to Queen Bluegarden. She reveals the Bluegarden that rules Ivor Tower is a robotic imposter that imprisoned her and moved the kingdom across the land to rule them in her place. The boy returns to Ivor Tower and destroys the fake Queen's minion, Mungola, and the Queen destroys herself when she crashes through the floor and is destroyed. The townsfolk return to Ebon Keep, and Bluegarden's inventor, Tinker, says he can help the boy return to the space station. The boy uses Tinker's flying machine to gather the needed parts from Prehistoria and Antiqua to build a rocket, and is launched to the space station, Omnitopia.

At the station the boy meets with Professor Ruffleberg. Ruffleberg explains that he conducted his experiment 30 years ago, but they have all been trapped in the simulation, called Evermore, by the machinations of Ruffleberg's robotic butler, Carltron. Carltron sabotaged the experiment to strand them in Evermore, and has recently attempted to use robot duplicates of Ruffleberg's friends to take control of Evermore for himself. The boy returns to Gothica to retrieve Aegis' dormant power core and uses it to activate a teleporter to Carltron's lair. The boy destroys Carltron's strongest robots, and Ruffleberg finally deactivates him.

With Carltron deactivated, Evermore begins to de-stabilize as his influence on the world has been lost, and cataclysms break out across the planet. The boy quickly returns to the surface to gather Elizabeth, Horace, and Bluegarden, and return to Omnitopia. Ruffleberg returns all of them to the real world, and the boy awakens outside the movie theater, where a movie "Secret of Evermore" is showing. The boy wonders if his adventure was all a dream brought on by a movie. At the mansion, Ruffleberg and his friends contemplate what will happen to Evermore without them, and how they will adapt to the new world after being gone for so long.

Secret of Evermore is an action-RPG where the player fights enemies in the field and moves around freely. The player controls the boy and his dog, able to switch control between them. The boy can equip numerous different types of weapons, each with different attack properties and special attacks. Alchemy serves as the game's equivalent of a magic system, combining two ingredients together to create various effects. Repeated usage of alchemy and weapons levels them up, increasing their power. The different weapon types are also needed to solve some puzzles; for instance, axe weapons can be used to crush barricades and break down some weak walls.

The boy - A normal kid from Podunk with a love of cheesy B-movies, the boy is drawn into Evermore and forced to fight his way out as he discovers what caused the experiment to go wrong. He wields various weapons and uses alchemy formulas as magic spells.

The dog - The boy's faithful dog, he changes breeds in each of Evermore's regions to more suit the area. He aids him in battle by biting and clawing enemies.

Elizabeth - Nicknamed "Fire Eyes" for how her eyes glow when she uses her magic, she is the ruler of Prehistoria and Ruffleberg's granddaughter.

Horace Highwater - The curator of the Podunk museum and a close friend of Ruffleberg, Horace makes camp in Antiqua to explore the ruins in the region.

Camellia Bluegarden - The ruler of the Gothica region and a librarian in Podunk, she was imprisoned by Carltron's doppelganger to usurp the kingdom.

Sydney Ruffleberg - A genius scientist, the creator of Evermore, and the ruler of Omnitopia.

Carltron - Ruffleberg's robotic butler, he grew tired of being a servant and sabotaged the experiment to trap the group in Evermore. It is his mind's influence that spawns the monsters in the world.

Cecil Harvey cameos in Ebon Keep as an innkeeper. He makes explicit references to the events of Final Fantasy IV, asking the boy if he has heard of him (if the player answers that they have heard of him at some point during his questions, Cecil offers a discount to the boy). After Zeromus's defeat, Cecil retired to Ebon Keep with Rosa to live out a quiet life.

The game was originally planned to be released under its core development name Evermore, but because Squaresoft was afraid a newly named IP would not catch on so easily, Secret of was added onto it. This is because the battles and gameplay bear more than a striking resemblance to Secret of Mana, which was released in the U.S. previously to impressive sales numbers and of which the North American-based development team borrowed various elements from. It was largely believed via rumors in gaming magazines that Secret of Evermore was the reason the U.S. never localized Seiken Densetsu 3, the only console Mana title that has never been officially released outside of Japan; of course this rumor has since been proven ultimately false.